How important is budding speciation for comparative studies?

The acknowledgment of evolutionary dependence among species has
fundamentally changed how we ask biological questions. Phylogenetic models
became the standard approach for studies with three or more lineages, in
particular those using extant species. Most phylogenetic comparative
methods (PCMs) translate relatedness into covariance, meaning that
evolutionary changes before lineages split should be interpreted together
whereas after the split lineages are expected to change independently.
This clever realization has shaped decades of research. Here we discuss
one element of the comparative method often ignored or assumed as
unimportant: if nodes of a phylogeny represent the dissolution of the
ancestral lineage into two new ones or if the ancestral lineage can
survive speciation events (i.e., budding). Budding speciation is often
reported in paleontological studies, due to the nature of the evidence for
budding in the fossil record, but it is surprisingly absent in comparative
methods. Here we show that many PCMs assume that divergence happens as a
symmetric split, even if these methods don’t explicitly mention this
assumption. We discuss the properties of trait evolution models for
continuous and discrete traits and their adequacy under a scenario of
budding speciation. We discuss the effects of budding speciation under a
series of plausible evolutionary scenarios and show when and how these can
influence our estimates. We also propose that long-lived lineages that
have survived through a series of budding speciation events and given
birth to multiple new lineages can produce evolutionary patterns that
challenge our intuition about the most parsimonious history of trait
changes in a clade. We hope our discussion can help bridge comparative
approaches in paleontology and neontology as well as foster awareness
about the assumptions we make when we use phylogenetic trees.